Hypopigmentation in mantled howler monkeys Alouatta palliata (gray 1849): First documented cases of whole‐body leucism in South America

Abstract The existence of hypopigmentation like leucism is the result of genetic anomalies that might be enhanced by external factors such as pollution. This anomaly may reduce survival rates. Leucism has been recorded in wildlife, but overall, it is considered very rare. There have been few records of mantled howler monkeys with leucism in Mexico and Costa Rica, but whole‐body leucism in howler monkeys from South America was unknown. In this article, we report for the first‐time documented cases of whole‐body leucism in young individuals of mantled howler monkeys Alouatta palliata in an isolated remanent of tropical dry forest in southwestern Ecuador known as Cerro Blanco Protective Forest. In total, we found two juvenile individuals with leucism in October 2021. The report of howler monkeys with whole‐body leucism may be caused by two processes: inbreeding because of isolated populations, environmental pressure caused by pollution, or the interaction of both. Our findings also reveal that hypopigmentation is becoming more frequent in howler monkey populations along its distributional range. Therefore, it is important to promote research in this field to disentangle the causes of hypopigmentation and to consider a regional management strategy for the species.

On the other hand, leucism is controlled by six genes (Reissmann & Ludwig, 2013); leucistic animals show partial or total loss of pigmentation in skin or fur but maintain normal coloration in the eyes or hands (García-Morales et al., 2012;Liu et al., 2019;Silva-Caballero et al., 2014). Vertebrates with these color aberrations are mostly reported in small and isolated populations, where inbreeding causes recessive alleles to be expressed (Bensch et al., 2000).
Survival rates of these animals are usually reported to be low (Owen & Skimmings, 1992).
Even though hypopigmentation is mainly gene driven, it is known that environmental stressors might enhance its occurrence. For example, some environmental aspects that are related to hypopigmentation are altered habitats (Kehas et al., 2005), diet (Coimbra-Filho & da Cruz Rocha, 1978;Peles et al., 1995) and pollution (Martin et al., 2022;Møller & Mousseau, 2001). Vertebrates color depend on two melanin molecules: eumelanin (polymers of indole units that promotes dark and gray colors) and pheomelanin (oligomers of sulfur-containing heterocycles promoting yellowish, reddish, chestnut and brown colors), produced by the melanocytes (Toral et al., 2008). Both molecules are present in all vertebrates and its proportion varies depending on the prevalence of the color patter of each species (Galvan & Solano, 2009). Besides the genetic control, the exposure to oxidative stress in the environment may shift the proportion of melanin molecules or even inhibit melanin production (Pang et al., 2014;Roulin et al., 2008), deriving in hypopigmentation.

The mantled howler monkey
Hypopigmentation in individuals of A. palliata has been reported previously in Mexico and Costa Rica (Galván et al., 2019;López-Platas et al., 2021;Ramos-Luna et al., 2022;Sánchez-Soto, 2018), but no record has been found in South America. In this nature note, to our knowledge, we present the first published report of mantled howler monkeys showing whole-body leucism in South America.
In total, we found two juvenile individuals in a private protected forest known as Cerro Blanco Protective Forest (CBPF) located in Guayaquil, Ecuador. We also hypothesized possible causes of this previously unrecorded phenomena.

| Description of site
The tropical dry forest is considered critically endangered worldwide (Ferrer-Paris et al., 2019). Locally, the ecosystem has lost over 70% of its original vegetation (Best & Kessler, 1995

| Description of mantled howler monkey (Alouatta palliata)
Mantled howler is a relatively big monkey with black whole-body coloration except for the flanks that may be yellowish, golden, or dull brown (Tirira, 2017). It is a diurnal, gregarious, and arboreal primate (Emmons & Feer, 1999) that feeds primarily on leaves. Nevertheless, it may also ingest fruits, nectar, and flowers (Crockett, 1998). Occasionally, insects may be consumed while ingesting plants (Tirira, 2008). The mantled howler monkey lives in groups usually from 2 to 18 members but in well-preserved forests, groups may be composed of more than 40 individuals. (Emmons & Feer, 1999;Tirira, 2017). Groups consist of one or more adult males, adult females, and young males and females (Chapman & Balcomb, 1998). Both young males and females are separated from the group before adulthood and live in solitary until they are able to join another group (Tirira, 2017).

| Observational methods
We observed the individuals opportunistically while doing research on rodents, plants, and birds. Therefore, no systematic method was applied.

| Observation of the first whole-body leucistic individual
We ( Figure 3). In all observations, the individual was at least 5 meters apart from the group.

| Observation of the second whole-body leucistic individual
We observed the second whole-body leucistic juvenile only once, on November 11th, 2021 at 8:42 a.m. EST for ~3 min at 612212 E -9760699 S. It was part of a group of seven individuals (composed of 2 juveniles and 5 adults) at approximately 14 meters high. There was a small chance to observe the individual and take photos because most of the time it stayed between the higher branches, as we described for first leucistic individual (Figure 4). The individual presented a white-to-gray pigmentation in its fur with dark-spotted palms and tail. sulfur-based pesticides, suggesting that sulfur is added to melanin molecules resulting in phaeomelanin. In this manuscript, we also hypothesized that the independent and simultaneous occurrence of two juvenile howler monkey with leucism in two separate groups might be also a result of exposure to pollution. In Guayaquil, there is evidence of high levels of sulfur (Quevedo et al., 2018) and heavy metals such as Zinc, Copper, Magnesium, Nickel and Chrome (Morales-Estupiñan et al., 2020). It is possible that one of these pollutants is promoting changes in melanogenesis pathways producing leucism in howler monkeys in Guayaquil. However, as this is not the scope of the research and the encounters were merely anecdotal, we are not able to confirm the causes of the phenomena.

| DISCUSS ION
In addition, we think that there might be an interaction between genetic drivers and environmental stressors that are causing hypopigmentation. It is known that oxidative stress caused by external agents such as pollution produces DNA damage directly affecting melanogenesis (Chen et al., 2021). In the case of the juveniles howler monkeys reported in this manuscript, the continuous presence of pollutants such as heavy metals and sulfur (Morales-Estupiñan et al., 2020;Quevedo et al., 2018) might cause oxidative stress in howler monkey individuals and possible other vertebrated, promoting pigmentation changes, similar to what has been hypothesized by Galván et al. (2019) in Costa Rica. We further think that the occurrence of this phenomena in the area is likely to increase in the next few years as the area surrounding CBPF is considered an area of urban expansion.
To our knowledge, the observation of the individuals represents the first documented cases of whole-body leucism for mantled howler monkeys in South America. This information contributes to what has been found in Mexico and Costa Rica (Galván et al., 2019;López-Platas et al., 2021;Ramos-Luna et al., 2022;Sánchez-Soto, 2018). Although our hypotheses are to an extent, speculative, as we were not able to capture any individuals to make further analysis (e.g., genetic, hair analysis), it is remarkable the importance to promote research in these fields to disentangle the causes of hypopigmentation (genetic pressure, environmental pressure, or the interaction of both) and to understand the effects of this phenomena over ecological and social behavior of the mantled howler monkeys. As a final recommendation, it is also very relevant to set regional strategies for the conservation of the mantled howler monkey that is considered vulnerable worldwide (Cortes-Ortíz et al., 2021) and critically endangered in Ecuador (Tirira, 2021).

ACK N OWLED G M ENTS
The authors are especially grateful to the Airport Authority of Guayaquil for funding the research. To Pro-Bosque Foundation for allowing us to carry out a scientific exploration in their area and a very special thanks to Paul Cun, Armando Manzaba, and Benito Choez for their unconditional and invaluable help during the sampling. We thank Zoila Vega, Anahí Vargas, and Rebeca Rivas for their valuable comments on this article. Finally, we really appreciate observations and language annotations done by Nicholas Dunn and Robyn Geldard.

DATA AVA I L A B I L I T Y S TAT E M E N T
Data sharing is not applicable to this article as no datasets were gen-